WASHINGTON — The leadership vacancy created by Homeland Security Secretary Janet Napolitano’s resignation is the latest and greatest blow to a department where one-third of the heads of key agencies and divisions have been filled with acting officials or remained vacant for months.

Napolitano’s departure, slated for September, will create the 15th hole in the department’s 45 leadership positions.

Napolitano’s chief of staff and director of Immigration and Customs Enforcement are leaving this month. The deputy secretary, general counsel, heads of Customs and Border Protection, privacy, legislative affairs, intelligence and analysis and more are filled with acting officials. Other key positions — executive secretariat, inspector general and deputy undersecretary for cybersecurity — remain vacant.

The acting deputy secretary at the department is poised to take over as acting secretary unless the Senate confirms the president’s nominee for Homeland Security deputy secretary before Napolitano leaves.

This swath of vacancies raises questions about how a department depleted of permanent leadership could implement changes, particularly as Congress considers overhauling the immigration system.

“Her departure is a substantial addition to the growing list of unfilled key leadership positions within the department,” said Rep. Michael McCaul, R-Texas, who is chairman of the House Homeland Security Committee. “The administration should move swiftly to fill the gaping holes in its management.”

The White House referred a request for comment to the department, which did not respond.

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